Abstract
Pleiotropy allows for the deterministic fixation of bidirectional mutations: mutations with effects both in the direction of selection and opposite to selection for the same character. Mutations with deleterious effects on some characters can fix because of beneficial effects on other characters. This study analytically quantifies the expected frequency of mutations that fix with negative and positive effects on a character and the average size of a fixed effect on a character when a mutation pleiotropically affects from very few to many characters. The analysis allows for mutational distributions that vary in shape and provides a framework that would allow for varying the frequency at which mutations arise with deleterious and positive effects on characters. The results show that a large fraction of fixed mutations will have deleterious pleiotropic effects even when mutation affects as little as two characters and only directional selection is occurring, and, not surprisingly, as the degree of pleiotropy increases the frequency of fixed deleterious effects increases. As a point of comparison, we show how stabilizing selection and random genetic drift affect the bidirectional distribution of fixed mutational effects. The results are then applied to QTL studies that seek to find loci that contribute to phenotypic differences between populations or species. It is shown that QTL studies are biased against detecting chromosome regions that have deleterious pleiotropic effects on characters.
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Selected References
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- Bradshaw H. D., Jr, Otto K. G., Frewen B. E., McKay J. K., Schemske D. W. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics. 1998 May;149(1):367–382. doi: 10.1093/genetics/149.1.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doebley J., Stec A. Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics. 1993 Jun;134(2):559–570. doi: 10.1093/genetics/134.2.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill W. G., Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966 Dec;8(3):269–294. [PubMed] [Google Scholar]
- Lyman R. F., Lawrence F., Nuzhdin S. V., Mackay T. F. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996 May;143(1):277–292. doi: 10.1093/genetics/143.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macdonald S. J., Goldstein D. B. A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics. 1999 Dec;153(4):1683–1699. doi: 10.1093/genetics/153.4.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mackay T. F., Lyman R. F., Jackson M. S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics. 1992 Feb;130(2):315–332. doi: 10.1093/genetics/130.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noor M. A., Cunningham A. L., Larkin J. C. Consequences of recombination rate variation on quantitative trait locus mapping studies. Simulations based on the Drosophila melanogaster genome. Genetics. 2001 Oct;159(2):581–588. doi: 10.1093/genetics/159.2.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orr H. A. Adaptation and the cost of complexity. Evolution. 2000 Feb;54(1):13–20. doi: 10.1111/j.0014-3820.2000.tb00002.x. [DOI] [PubMed] [Google Scholar]
- Orr H. A. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics. 1998 Aug;149(4):2099–2104. doi: 10.1093/genetics/149.4.2099. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orr H. A. The evolutionary genetics of adaptation: a simulation study. Genet Res. 1999 Dec;74(3):207–214. doi: 10.1017/s0016672399004164. [DOI] [PubMed] [Google Scholar]
- Otto S. P., Jones C. D. Detecting the undetected: estimating the total number of loci underlying a quantitative trait. Genetics. 2000 Dec;156(4):2093–2107. doi: 10.1093/genetics/156.4.2093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rieseberg Loren H., Widmer Alex, Arntz A. Michele, Burke John M. The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos Trans R Soc Lond B Biol Sci. 2003 Jun 29;358(1434):1141–1147. doi: 10.1098/rstb.2003.1283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tanksley S. D. Mapping polygenes. Annu Rev Genet. 1993;27:205–233. doi: 10.1146/annurev.ge.27.120193.001225. [DOI] [PubMed] [Google Scholar]